1887
No metrics data to plot.
The attempt to load metrics for this article has failed.
The attempt to plot a graph for these metrics has failed.

EcoSal Plus

Domain 3:

Metabolism

Biosynthesis of Proline

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.
Buy article
Choose downloadable ePub or PDF files.
Buy this Chapter
Digital (?) $30.00
  • Authors: Laszlo N. Csonka1, and Thomas Leisinger2
  • Editor: Valley Stewart3
  • VIEW AFFILIATIONS HIDE AFFILIATIONS
    Affiliations: 1: Department of Biological Sciences, Purdue University, West Lafayette, IN 47907-1392; 2: Institut für Mikrobiologie, Wolfgang Pauli Strasse 10, CH-8093 Zürich, Switzerland; 3: University of California, Davis, Davis, CA
  • Received 09 May 2006 Accepted 12 July 2006 Published 08 August 2007
  • Address correspondence to Laszlo N. Csonka lcsonka@bio.purdue.edu
image of Biosynthesis of Proline
    Preview this reference work article:
    Zoom in
    Zoomout

    Biosynthesis of Proline, Page 1 of 2

    | /docserver/preview/fulltext/ecosalplus/2/2/3_6_1_4_module-1.gif /docserver/preview/fulltext/ecosalplus/2/2/3_6_1_4_module-2.gif
  • Abstract:

    Proline was among the last biosynthetic precursors to have its biosynthetic pathway unraveled. This review recapitulates the findings on the biosynthesis and transport of proline. Glutamyl kinase (GK) catalyzes the ATP-dependent phosphorylation of L-glutamic acid. Purification of γ-GK from was facilitated by the expression of the and genes from a high-copy-number plasmid and the development of a specific coupled assay based on the NADPH-dependent reduction of GP by γ-glutamyl phosphate reductase (GPR). GPR catalyzes the NADPH-dependent reduction of GP to GSA. Site directed mutagenesis was used to identify residues that constitute the active site of GK. This analysis indicated that there is an overlap between the binding sites for glutamate and the allosteric inhibitor proline, suggesting that proline competes with the binding of glutamate. The review also summarizes the genes involved in the metabolism of proline in and . Among the completed genomic sequences of , genes specifying all three proline biosynthetic enzymes can be discerned in , , , , , , , and strain morsitans. The intracellular proline concentration increases with increasing external osmolality in proline-overproducing mutants. This apparent osmotic regulation of proline accumulation in the overproducing strains may be the result of increased retention or recapture of proline, achieved by osmotic stimulation of the ProP or ProU proline transport systems. A number of proline analogs can be incorporated into proteins in vivo or in vitro.

  • Citation: Csonka L, Leisinger T. 2007. Biosynthesis of Proline, EcoSal Plus 2007; doi:10.1128/ecosalplus.3.6.1.4

References

1. Tomenchok DM, Brandriss MC. 1987. Gene-enzyme relationships in the proline biosynthetic pathway of Saccharomyces cerevisiae. J Bacteriol 169:5364–5372.[PubMed]
2. Tristram H. 1972. Some aspects of the regulation of amino acid biosynthesis in bacteria. Annu Proc Phytochem Soc 9:21–48.
3. Papas TS, Mehler AH. 1971. Kinetic studies of the prolyl transfer ribonucleic acid synthetase of Escherichia coli. J Biol Chem 246:5924–5928.[PubMed]
4. Shibasaki T, Mori H, Ozaki A. 2000. Enzymatic production of trans-4-hydroxy-L-proline by regio- and stereospecific hydroxylation of L-proline. Biosci Biotechnol Biochem 64:746–750. [PubMed][CrossRef]
5. Baich A, Pierson DJ. 1965. Control of proline synthesis in Escherichia coli. Biochim Biophys Acta 104:397–404.[PubMed]
6. Baich A. 1971. The biosynthesis of proline in Escherichia coli: phosphate-dependent glutamate-semialdehyde dehydrogenase (NADP), the second enzyme in the pathway. Biochim Biophys Acta 244:129–134.[PubMed]
7. Belitsky BR, Brill J, Bremer E, Sonenshein AL. 2001. Multiple genes for the last step of proline biosynthesis in Bacillus subtilis. J Bacteriol 183:4389–4392. [PubMed][CrossRef]
8. Kim W, George A, Evans M, Conticello VP. 2004. Cotranslational incorporation of a structurally diverse series of proline analogues in an Escherichia coli expression system. Chembiochem 5:928–936. [PubMed][CrossRef]
9. Krishna RV, Beilstein P, Leisinger T. 1979. Biosynthesis of proline in Pseudomonas aeruginosa. Properties of γ-glutamylphosphate reductase and 1-pyrroline-5-carboxylate reductase. Biochem J 181:223–230.[PubMed]
10. Rossi JJ, Berg CM. 1971. Differential recovery of auxotrophs after penicillin enrichment in Escherichia coli. J Bacteriol 106:297–300.[PubMed]
11. Smith CJ, Deutch AH, Rushlow KE. 1984. Purification and characteristics of a γ-glutamyl kinase involved in Escherichia coli proline biosynthesis. J Bacteriol 157:545–551.[PubMed]
12. Delauney AJ, Hu CA, Kishor PB, Verma DP. Cloning of ornithine δ-aminotransferase cDNA from Vigna aconitifolia by trans-complementation in Escherichia coli and regulation of proline biosynthesis. J Biol Chem 268:18673–18678.
13. Adams E, Frank L. 1980. Metabolism of proline and the hydroxyprolines. Annu Rev Biochem 49:1005–1061. [PubMed][CrossRef]
14. Lee M-L, Muench KH. 1969. Prolyl transfer ribonucleic acid synthetase of Escherichia coli. J Biol Chem 244:223–230.[PubMed]
15. Baich A. 1969. Proline synthesis in Escherichia coli. A proline-inhibitable glutamic acid kinase. Biochim Biophys Acta 192:462–467.[PubMed]
16. Hayzer DJ, Krishna RV, Margraff R. 1979. Enzymic synthesis of glutamic acid γ-semialdehyde (Δ1-pyrroline-5-carboxylate) and N-acetyl-L-glutamic acid γ-semialdehyde: isolation and characterization of their 2,4-dinitrophenylhydrazones. Anal Biochem 96:94–103. [PubMed][CrossRef]
17. Kaback HR, Deuel TF. 1969. Proline uptake by disrupted membrane preparations from Escherichia coli. Arch Biochem Biophys 132:118–129. [PubMed][CrossRef]
18. Hayzer DJ, Leisinger T. 1983. Proline biosynthesis in Escherichia coli. Kinetic and mechanistic properties of glutamate semialdehyde dehydrogenase. Biochim Biophys Acta 742:391–398.[PubMed]
19. Rowland I, Tristram H. 1975. Specificity of the Escherichia coli proline transport system. J Bacteriol 123:871–877.[PubMed]
20. Hayzer DJ, Leisinger T. 1980. The gene-enzyme relationships of proline biosynthesis in Escherichia coli. J Gen Microbiol 118:287–293.[PubMed]
21. Seddon A, Zhao KY, Meister A. 1989. Activation of glutamate by γ-glutamyl kinase: formation of γ-cis-cycloglutamyl phosphate, an analog of γ-glutamyl phosphate. J Biol Chem 264:11326–11335.[PubMed]
22. Serebrijski I, Reyes O, Leblon G. 1995. Corrected gene assignments of Escherichia coli Pro mutations. J Bacteriol 177:7261–7264.[PubMed]
23. Hernandez PE, Ordonez JA, Perez BS. 1983. Use of the Mud(Ap, lac) bacteriophage to study the regulation of L-proline biosynthetic genes in Escherichia coli K-12. Curr Microbiol 9:31–35. [CrossRef]
24. Deutch AH, Rushlow KE, Smith CJ. 1984. Analysis of the Escherichia coli proBA locus by DNA and protein sequencing. Nucleic Acids Res 12:6337–6355. [PubMed][CrossRef]
25. Parkhill J, Dougan G, James KD, Thomson NR, Pickard D, Wain J, Churcher C, Mungall KL, Bentley SD, Holden MT, Sebaihia M, Baker S, Basham D, Brooks K, Chillingworth T, Connerton P, Cronin A, Davis P, Davies RM, Dowd L, White N, Farrar J, Feltwell T, Hamlin N, Haque A, Hien TT, Holroyd S, Jagels K, Krogh A, Larsen TS, Leather S, Moule S, O'Gaora P, Parry C, Quail M, Rutherford K, Simmonds M, Skelton J, Stevens K, Whitehead S, Barrell BG. 2001. Complete genome sequence of a multiple drug resistant Salmonella enterica serovar Typhi. Nature 413:848–852. [PubMed][CrossRef]
26. Sugiura M, Kisumi M. 1985. Proline-hyperproducing strains of Serratia marcescens: enhancement of proline analog-mediated growth inhibition by increasing osmotic stress. Appl Environ Microbiol 49:782–786.[PubMed]
27. Fujita T, Maggio A, García-Ríos M, Bressan RA, Csonka LN. 1998. Comparative analysis of the regulation of expression and structures of two evolutionarily divergent genes for Δ1-pyrroline-5-carboxylate synthetase from tomato. Plant Physiol 118:661–674. [PubMed][CrossRef]
28. Mori H, Shibasaki T, Yano K, Ozaki A. 1997. Purification and cloning of a proline 3-hydroxylase, a novel enzyme which hydroxylates free L-proline to cis-3-hydroxy-L-proline. J Bacteriol 179:5677–5683.[PubMed]
29. Aravind L, Koonin EV. 1999. Novel predicted RNA-binding domains associated with the translation machinery. J Mol Evol 48:291–302. [PubMed][CrossRef]
30. Liao MK, Gort S, Maloy S. 1997. A cryptic proline permease in Salmonella typhimurium. Microbiology 143:2903–2911. [PubMed][CrossRef]
31. Mahan MJ, Csonka LN. 1983. Genetic analysis of the proBA genes of Salmonella typhimurium; physical and genetic analyses of the cloned proB+A+ genes of Escherichia coli and of a mutant allele that confers proline overproduction and increased osmotolerance. J Bacteriol 156:1249–1262.[PubMed]
32. Rushlow KE, Deutch AH, Smith CJ. 1985. Identification of a mutation that relieves gamma-glutamyl kinase from allosteric feedback inhibition by proline. Gene 39:109–112. [PubMed][CrossRef]
33. Omori K, Suzuki S-I, Imai Y, Komatsubara S. 1991. Analysis of the Serratia marcescens proBA operon and feedback control of proline biosynthesis. J Gen Microbiol 137:509–517.[PubMed]
34. Stalmach ME, Grothe S, Wood JM. 1983. Two proline porters in Escherichia coli K-12. J Bacteriol 156:481–486.[PubMed]
35. Tristram H, Thurston CF. 1966. Control of proline biosynthesis by proline and proline analogues. Nature (London) 212:74–75. [CrossRef]
36. Williams I, Frank L. 1975. Improved chemical synthesis and enzymatic assay of Δ1-pyrroline-5-carboxylic acid. Anal Biochem 64:85–97. [PubMed][CrossRef]
37. Hasegawa T, Yokogawa T. 2000. Escherichia coli proline tRNA: structure and recognition sites for prolyl-tRNA synthetase. Nucleic Acids Symp Ser 2000:7–8.
38. Hayzer DJ, Leisinger T. 1982. Proline biosynthesis in Escherichia coli: purification and characterization of glutamate-semialdehyde dehydrogenase. Eur J Biochem 121:561–565. [PubMed][CrossRef]
39. Measures JC. 1975. Role of amino acids in osmoregulation of nonhalophilic bacteria. Nature (London) 257:398–400. [CrossRef]
40. Savioz A, Jeenes DJ, Kocher HP, Haas D. 1990. Comparison of proC and other housekeeping genes of Pseudomonas aeruginosa with their counterparts in Escherichia coli. Gene 86:107–111. [PubMed][CrossRef]
41. Hayzer DJ, Leisinger T. 1981. Proline biosynthesis in Escherichia coli. Stoichiometry and end-product identification of the reaction catalysed by glutamate semialdehyde dehydrogenase. Biochem J 197:269–274.[PubMed]
42. Quick M, Tebbe S, Jung H. 1996. Ser57 in the Na+/proline permease of Escherichia coli is critical for high-affinity proline uptake. Eur J Biochem 239:732–736. [PubMed][CrossRef]
43. Deutch AH, Smith CJ, Rushlow KE, Kretschmer PJ. 1982. Escherichia coli Δ1-pyrroline-5-carboxylate reductase: gene sequence, protein overproduction and purification. Nucleic Acids Res 10:7701–7714. [PubMed][CrossRef]
44. Berg CM, Rossi JJ. 1974. Proline excretion and indirect suppression in Escherichia coli and Salmonella typhimurium. J Bacteriol 118:928–939.[PubMed]
45. Inuzuka M, Toyama H, Miyano H, Tomoeda M. 1976. Specific action of 4-nitropyridine 1-oxide on Escherichia coli K-12 Pro+ strains leading to the isolation of proline-requiring mutants: mechanism of action of 4-nitropyridine 1-oxide. Antimicrob Agents Chemother 10:333–343.[PubMed]
46. Kuchino Y, Yabusaki Y, Mori F, Nishimura S. 1984. Nucleotide sequences of three proline tRNAs from Salmonella typhimurium. Nucleic Acids Res 12:1559–1562. [PubMed][CrossRef]
47. Eckhardt T, Leisinger T. 1975. Isolation and characterization of mutants with a feedback resistant N-acetylglutamate synthase in Escherichia coli K12. Mol Gen Genet 138:225–232. [PubMed][CrossRef]
48. Hu C-AA, Delauney AJ, Verma DPS. 1992. A bifunctional enzyme (Δ1-pyrroline-5-carboxylate synthetase) catalyzes the first two steps in proline biosynthesis in plants. Proc Natl Acad Sci USA 89:9354–9358. [PubMed][CrossRef]
49. Quick M, Stolting S, Jung H. 1999. Role of conserved Arg40 and Arg117 in the Na+/proline transporter of Escherichia coli. Biochemistry 38:13523–13529. [PubMed][CrossRef]
50. Omori K, Suzuki S, Imai Y, Komatsubara S. 1992. Analysis of the mutant proBA operon from a proline producing strain of Serratia marcescens. J Gen Microbiol 138:693–699.[PubMed]
51. MacMillan SV, Alexander DA, Culham DE, Kunte HJ, Marshall EV, Rochon D, Wood JM. 1999. The ion coupling and organic substrate specificities of osmoregulatory transporter ProP in Escherichia coli. Biochim Biophys Acta 1420:30–44. [PubMed][CrossRef]
52. Limauro D, Falciatore A, Basso AL, Forlani G, De Felice M. 1996. Proline biosynthesis in Streptococcus thermophilus: characterization of the proBA operon and its products. Microbiology 142:3275–3282. [PubMed][CrossRef]
53. Britten RJ, McClure FT. 1962. The amino acid pool in Escherichia coli. Bacteriol Rev 26:292–335.[PubMed]
54. Massarelli I, Forlani G, Ricca E, DeFelice M. 2000. Enhanced and feedback resistant γ-glutamyl kinase activity of an Escherichia coli transformant carrying a mutated proB gene of Streptococcus thermophilus. FEMS Microbiol Lett 182:143–147. [PubMed][CrossRef]
55. Csonka LN. 1981. Proline overproduction results in enhanced osmotolerance in Salmonella typhimurium. Mol Gen Genet 182:82–86. [PubMed][CrossRef]
56. Csonka LN. 1988. Regulation of the cytoplasmic proline levels of Salmonella typhimurium: effect of osmotic stress on the synthesis, degradation, and cellular retention of proline. J Bacteriol 170:2374–2378.[PubMed]
57. Smith LT. 1985. Characterization of a γ-glutamyl kinase from Escherichia coli that confers proline overproduction and osmotic tolerance. J Bacteriol 164:1088–1093.[PubMed]
58. Bloom F, Smith CJ, Jessee J, Veilleux B, Deutch AH. 1983. The use of genetically engineered strains of Escherichia coli for the overproduction of free amino acids: proline as a model system, p 383–394. In Downey K, Voellmy RW, Ahmad F, and Schultz J (ed), Advances in Gene Technology: Molecular Genetics of Plants and Animals. Academic Press, Orlando, Fla.
59. Brady RA, Csonka LN. 1988. Transcriptional regulation of the proC gene of Salmonella typhimurium. J Bacteriol 170:2379–2382.[PubMed]
60. Condamine H. 1971. Sur la régulation de la production de proline chez E. coli K12. Ann Inst Pasteur 120:126–143.
61. Hayzer DJ, Moses V. 1978. The enzymes of proline biosynthesis in Escherichia coli. Their molecular weights and the problem of enzyme aggregation. Biochem J 173:219–228.[PubMed]
62. Deutch CE, Klarstrom JL, Link CL, Ricciardi DL. 2001. Oxidation of L-thiazolidine-4-carboxylate by Δ1-pyrroline-5-carboxylate reductase in Escherichia coli. Curr Microbiol 42:442–446. [PubMed][CrossRef]
63. Vogel HJ, Davis BD. 1952. Glutamic γ-semialdehyde and Δ1-pyrroline-5-carboxylic acid, intermediates in the biosynthesis of proline. J Am Chem Soc 74:109–112. [CrossRef]
64. Tempest DW, Meers JL, Brown CM. 1970. Influence of environment on the content and composition of microbial free amino acid pools. J Gen Microbiol 64:171–185.[PubMed]
65. Quick M, Jung H. 1997. Aspartate 55 in the Na+/proline permease of Escherichia coli is essential for Na+-coupled proline uptake. Biochemistry 36:4631–4636. [PubMed][CrossRef]
66. Anderson RR, Menzel R, Wood JM. 1980. Biochemistry and regulation of a second L-proline transport system in Salmonella typhimurium. J Bacteriol 141:1071–1076.[PubMed]
67. Csonka LN. 1983. A third L-proline permease in Salmonella typhimurium which functions in media of elevated osmotic strength. J Bacteriol 151:1433–1443.
68. Grothe S, Krogsrud RL, McClellan DJ, Milner JL, Wood JM. 1986. Proline transport and osmotic stress response in Escherichia coli K-12. J Bacteriol 166:253–259.[PubMed]
69. Baich A, Smith FI. 1968. The effect of azetidine-2-carboxylic acid on the synthesis of proline in Escherichia coli. Experientia 15:1107. [CrossRef]
70. Grant MM, Brown AS, Corwin LM, Troxler RF, Franzblau C. 1975. Effect of L-azetidine 2-carboxylic acid on growth and proline metabolism in Escherichia coli. Biochim Biophys Acta 404:180–187.[PubMed]
71. Katchalsy A, Paecht M. 1954. Phosphate anhydrides of amino acids. J Am Chem Soc 76:6042–6044. [CrossRef]
72. Ratzkin B, Grabnar M, Roth J. 1978. Regulation of the major proline permease of Salmonella typhimurium. J Bacteriol 133:737–743.[PubMed]
73. Strecker HJ. 1957. The interconversion of glutamic acid and proline. I. The formation of Δ1 pyrroline-5-carboxylic acid from glutamic acid in Escherichia coli. J Biol Chem 225:825–834.[PubMed]
74. Di Girolamo M, Cini C, Busiello V, Coccia R, de Marco C. 1984. Thiaproline and selenaproline transport in E. coli. Physiol Chem Phys Med NMR 16:75–82.
75. Busiello V, Di Girolamo M, Cini C, De Marco C. 1979. Action of thiazolidine-2-carboxylic acid, a proline analog, on protein synthesizing systems. Biochim Biophys Acta 564:311–321.[PubMed]
76. De Marco C, Busiello V, Di Girolamo M, Cavallini D. 1977. Selenaproline and protein synthesis. Biochim Biophys Acta 478:156–166.[PubMed]
77. Gouesbet G, Jebbar M, Talibart R, Bernard T, Blanco C. 1994. Pipecolic acid is an osmoprotectant for Escherichia coli taken up by the general osmoporters ProU and ProP. Microbiology 140:2415–2422. [PubMed][CrossRef]
78. Fujita T, Maggio A, García-Ríos M, Stauffacher C, Bressan RA, Csonka LN. 2003. Identification of regions of the tomato γ-glutamyl kinase that are involved in allosteric regulation by proline. J Biol Chem 278:14203–14210. [PubMed][CrossRef]
79. Csonka LN, Gelvin SB, Goodner BW, Orser CS, Siemieniak D, Slightom JL. 1988. Nucleotide sequence of a mutation in the proB gene of Escherichia coli that confers proline overproduction and enhanced tolerance of osmotic stress. Gene 64:199–205. [PubMed][CrossRef]
80. Dandekar AM, Uratsu SL. 1988. A single base pair change in proline biosynthesis genes causes osmotic stress tolerance. J Bacteriol 170:5943–5945.[PubMed]
81. Ratzkin B, Roth J. 1978. Cluster of genes controlling proline degradation in Salmonella typhimurium. J Bacteriol 133:737–754.[PubMed]
82. Schiefner A, Breed J, Bösser L, Kneip S, Gade J, Holtmann G, Diederichs K, Welte W, Bremer E. 2004. Cation-π interactions as determinants for binding of the compatible solutes glycine betaine and proline betaine by the periplasmic ligand-binding protein ProX from Escherichia coli. J Biol Chem 279:5588–5596. [PubMed][CrossRef]
83. Milner JL, Grothe S, Wood JM. 1988. Proline porter II is activated by a hyperosmotic shift in both whole cells and membrane vesicles of Escherichia coli K-12. J Biol Chem 263:14900–14905.[PubMed]
84. Kuo T-T, Stocker BAD. 1969. Suppression of proline requirement of proA and proAB deletion mutants in Salmonella typhimurium by mutation to arginine requirement. J Bacteriol 98:593–598.[PubMed]
85. Eriani G, Delarue M, Poch O, Gangloff J, Moras D. 1990. Partition of tRNA synthetases into two classes based on mutually exclusive sets of sequence motifs. Nature (London) 347:293–206. [CrossRef]
86. Papas TS, Mehler AH. 1970. Analysis of the amino acid binding to the proline transfer ribonucleic acid synthetase of Escherichia coli. J Biol Chem 245:1588–1595.[PubMed]
87. Overdier DG, Csonka LN. 1992. A transcriptional silencer downstream of the promoter in the osmotically controlled proU operon of Salmonella typhimurium. Proc Natl Acad Sci USA 89:3140–3144. [PubMed][CrossRef]
88. Verbruggen N, VanMontagu M, Messens E. 1992. Synthesis of the proline analogue [2,3-3H]azetidine-2-carboxylic acid: uptake and incorporation in Arabidopsis thaliana and Escherichia coli. FEBS Lett 308:261–263. [PubMed][CrossRef]
89. Ahel I, Stathopoulos C, Ambrogelly A, Sauerwald A, Toogood H, Hartsch T, Söll D. 2002. Cysteine activation is an inherent in vitro property of prolyl-tRNA synthetases. J Biol Chem 277:34743–34748. [PubMed][CrossRef]
90. Bohman K, Isaksson LA. 1980. A temperature-sensitive mutant in prolinyl-tRNA ligase of Escherichia coli K-12. Mol Gen Genet 177:603–605. [PubMed][CrossRef]
91. Archibold ER, Williams LS. 1972. Regulation of synthesis of methionyl-, prolyl-, and threonyl-transfer ribonucleic acid synthetases of Escherichia coli. J Bacteriol 109:1020–1026.
92. Krishna RV, Leisinger T. 1979. Biosynthesis of proline in Pseudomonas aeruginosa. Partial purification and characterization of γ-glutamyl kinase. Biochem J 181:215–222.[PubMed]
93. Grunberg-Manago M. 1996. Regulation of the expression of aminoacyl-tRNA synthetases and translation factors, p 1432–1457. In Neidhardt FC, Curtiss R III, Ingraham JL, Lin ECC, Low KB, Magasanik B, Reznikoff WS, Riley M, Schaechter M, and Umbarger HE (ed), Escherichia coli and Salmonella: Cellular and Molecular Biology, 2nd ed. ASM Press, Washington, D.C.
94. Wong FC, Beuning PJ, Nagan M, Shiba K, Musier-Forsyth K. 2002. Functional role of the prokaryotic proline-tRNA synthetase insertion domain in amino acid editing. Biochemistry 41:7108–7115. [CrossRef]
95. Quick M, Jung H. 1998. A conserved aspartate residue, Asp187, is important for Na+-dependent proline binding and transport by the Na+/proline transporter of Escherichia coli. Biochemistry 37:13800–13806. [PubMed][CrossRef]
96. Csonka LN, Epstein W. 1996. Osmoregulation, p 1210–1223. In Neidhardt FC, Curtiss R III, Ingraham JL, Lin ECC, Low KB, Magasanik B, Reznikoff WS, Riley M, Schaechter M, and Umbarger HE (ed), Escherichia coli and Salmonella: Cellular and Molecular Biology, 2nd ed. ASM Press, Washington, D.C.
97. Druger-Liotta J, Prange VJ, Overdier DG, Csonka LN. 1986. Selection of mutations that alter the osmotic control of transcription of the Salmonella typhimurium proU operon. J Bacteriol 169:2449–2459.
98. Leisinger T. 1996. Biosynthesis of proline, p 434–441. In Neidhardt FC, Curtiss R III, Ingraham JL, Lin ECC, Low KB, Magasanik B, Reznikoff WS, Riley M, Schaechter M, and Umbarger HE (ed), Escherichia coli and Salmonella: Cellular and Molecular Biology, 2nd ed. ASM Press, Washington, D.C.
99. Jebbar M, Talibart R, Gloux K, Bernard T, Blanco C. 1992. Osmoprotection of Escherichia coli by ectoine: uptake and accumulation characteristics. J Bacteriol 174:5027–5035.[PubMed]
100. Jeschke G, Wegener C, Nietschke M, Jung H, Steinhoff HJ. 2004. Interresidual distance determination by four-pulse double electron-electron resonance in an integral membrane protein: the Na+/proline transporter PutP of Escherichia coli. Biophys J 86:2551–2557. [PubMed][CrossRef]
101. Jung H. 1998. Topology and function of the Na+/proline transporter of Escherichia coli, a member of the Na+/solute cotransporter family. Biochim Biophys Acta 1365:60–64. [PubMed][CrossRef]
102. Jung H, Rubenhagen R, Tebbe S, Leifker K, Tholema N, Quick M, Schmid R. 1998. Topology of the Na+/proline transporter of Escherichia coli. J Biol Chem 273:26400–26407. [PubMed][CrossRef]
103. Patte JC. 1996. Biosynthesis of threonine and lysine, p 528–541. In Neidhardt FC, Curtiss R III, Ingraham JL, Lin ECC, Low KB, Magasanik B, Reznikoff WS, Riley M, Schaechter M, and Umbarger HE (ed), Escherichia coli and Salmonella: Cellular and Molecular Biology, 2nd ed. ASM Press, Washington, D.C.
104. Pérez-Arellano I, Gil-Ortiz F, Cervera J, Rubio V. 2004. Glutamate-5-kinase from Escherichia coli: gene cloning, overexpression, purification and crystallization of the recombinant enzyme and preliminary X-ray studies. Acta Crystallogr D 60:2091–2094. [PubMed][CrossRef]
105. Pérez-Arellano I, Rubio V, Cervera J. 2006. Mapping active site residues in glutamate-5-kinase. The substrate glutamate and the feedback inhibitor proline bind at overlapping sites. FEBS Lett 580:6247–6253. [PubMed][CrossRef]
106. Pirch T, Landmeier S, Jung H. 2003. Transmembrane domain II of the Na+/proline transporter PutP of Escherichia coli forms part of a conformationally flexible, cytoplasmic exposed aqueous cavity within the membrane. J Biol Chem 278:42942–42949. [PubMed][CrossRef]
107. Pirch T, Quick M, Nietschke M, Langkamp M, Jung H. 2002. Sites important for Na+ and substrate binding in the Na+/proline transporter of Escherichia coli, a member of the Na+/solute symporter family. J Biol Chem 277:8790–8796. [PubMed][CrossRef]
108. Poolman B, Spitzer JJ, Wood JM. 2004. Bacterial osmosensing: roles of membrane structure and electrostatics in lipid-protein and protein-protein interactions. Biochim Biophys Acta 1666:88–104. [PubMed][CrossRef]
109. Wood JM. 1981. Genetics of L-proline utilization in Escherichia coli. J Bacteriol 146:895–901.[PubMed]
110. Meijer P-J, Lilius G, Holmberg N, Bülow L. 1996. An artificial bifunctional enzyme, γ-glutamyl kinase/γ-glutamyl phosphate reductase, improves NaCl tolerance when expressed in Escherichia coli. Biotechnol Lett 18:1133–1138. [CrossRef]
111. Serebrijski I, Wojcik F, Reyes O, Leblon G. 1995. Multicopy suppression by asd gene and osmotic stress-dependent complementation by heterologous proA in proA mutants. J Bacteriol 177:7255–7260.[PubMed]
112. Lisser S, Margalit H. 1993. Compilation of E. coli mRNA promoter sequences. Nucleic Acids Res 21:1507–1516. [PubMed][CrossRef]
113. Jung H, Tebbe S, Schmid R, Jung K. 1998. Unidirectional reconstitution and characterization of purified Na+/proline transporter of Escherichia coli. Biochemistry 37:11083–11088. [PubMed][CrossRef]
114. Dunlap VJ, Csonka LN. 1985. Osmotic regulation of L-proline transport in Salmonella typhimurium. J Bacteriol 163:296–304.
115. Menzel R, Roth J. 1980. Identification and mapping of a second proline permease in Salmonella typhimurium. J Bacteriol 141:1064–1070.[PubMed]
116. Pérez-Arellano I, Rubio V, Cervera J. 2005. Dissection of Escherichia coli glutamate 5-kinase: functional impact of the deletion of the PUA domain. FEBS Lett 579:6903–6908. [PubMed][CrossRef]
117. Vogel RH, Kopac MJ. 1959. Glutamic γ-semialdehyde in arginine and proline synthesis of Neurospora: a mutant-tracer analysis. Biochim Biophys Acta 36:505–510. [CrossRef]
118. Culham DE, Henderson J, Crane RA, Wood JM. 2003. Osmosensor ProP of Escherichia coli responds to the concentration, chemistry, and molecular size of osmolytes in the proteoliposome lumen. Biochemistry 42:410–420. [PubMed][CrossRef]
119. Cairney J, Booth IR, Higgins CF. 1985. Osmoregulation of gene expression in Salmonella typhimurium: proU encodes an osmotically induced betaine transport system. J Bacteriol 164:1224–1232.[PubMed]
120. Cairney J, Booth IR, Higgins CF. 1985. Salmonella typhimurium proP gene encodes a transport system for the osmoprotectant betaine. J Bacteriol 164:1218–1223.[PubMed]
121. Balaji B, O’Connor K, Lucas JR, Anderson JA, Csonka LN. 2005. Timing of induction of osmotically controlled genes in Salmonella enterica serovar Typhimurium determined with quantitative real-time reverse transcription-PCR. Appl Environ Microbiol 71:8273–8283. [PubMed][CrossRef]
122. Orser CS, Goodner BW, Johnston M, Gelvin SB, Csonka LN. 1988. The Escherichia coli proB gene corrects the proline auxotrophy of Saccharomyces cerevisiae pro1 mutants. Mol Gen Genet 212:124–128. [PubMed][CrossRef]
123. Rossi JJ, Vender J, Berg CM, Coleman WH. 1977. Partial purification and some properties of Δ1-pyrroline-5-carboxylate reductase from Escherichia coli. J Bacteriol 129:108–114.[PubMed]
124. Barron A, Jung JU, Villarejo M. 1987. Purification and characterization of a glycinebetaine binding protein from Escherichia coli. J Biol Chem 262:11841–11846.[PubMed]
125. Itikawa H, Baumberg S, Vogel HJ. 1968. Enzymic basis for a genetic suppression: accumulation and deacylation of N-acetylglutamic γ-semialdehyde in enterobacterial mutants. Biochim Biophys Acta 159:547–550.[PubMed]
126. Wood JM, Culham DE, Hillar A, Vernikovska YI, Liu F, Boggs JM, Keates RAB. 2005. A structural model for the osmosensor, transporter, and osmoregulator ProP of Escherichia coli. Biochemistry 44:5634–5646. [PubMed][CrossRef]
127. Wu GY, Seifter S. 1975. A new method for the preparation of Δ1-pyrroline 5-carboxylic acid. Anal Biochem 67:413–421. [PubMed][CrossRef]
128. Yap LP, Stehlin C, Musier-Forsyth K. 1995. Use of semi-synthetic transfer RNAs to probe molecular recognition by Escherichia coli proline-tRNA synthetase. Chem Biol 2:661–666. [PubMed][CrossRef]
129. Zhou A, Wozniak A, Meyer-Lipp K, Nietschke M, Jung H, Fendler K. 2004. Charge translocation during cosubstrate binding in the Na+/proline transporter of E. coli. J Mol Biol 343:931–942. [PubMed][CrossRef]
ecosalplus.3.6.1.4.citations
ecosalplus/2/2
content/journal/ecosalplus/10.1128/ecosalplus.3.6.1.4
Loading

Citations loading...

Loading

Article metrics loading...

/content/journal/ecosalplus/10.1128/ecosalplus.3.6.1.4
2007-08-08
2017-05-24

Abstract:

Proline was among the last biosynthetic precursors to have its biosynthetic pathway unraveled. This review recapitulates the findings on the biosynthesis and transport of proline. Glutamyl kinase (GK) catalyzes the ATP-dependent phosphorylation of L-glutamic acid. Purification of γ-GK from was facilitated by the expression of the and genes from a high-copy-number plasmid and the development of a specific coupled assay based on the NADPH-dependent reduction of GP by γ-glutamyl phosphate reductase (GPR). GPR catalyzes the NADPH-dependent reduction of GP to GSA. Site directed mutagenesis was used to identify residues that constitute the active site of GK. This analysis indicated that there is an overlap between the binding sites for glutamate and the allosteric inhibitor proline, suggesting that proline competes with the binding of glutamate. The review also summarizes the genes involved in the metabolism of proline in and . Among the completed genomic sequences of , genes specifying all three proline biosynthetic enzymes can be discerned in , , , , , , , and strain morsitans. The intracellular proline concentration increases with increasing external osmolality in proline-overproducing mutants. This apparent osmotic regulation of proline accumulation in the overproducing strains may be the result of increased retention or recapture of proline, achieved by osmotic stimulation of the ProP or ProU proline transport systems. A number of proline analogs can be incorporated into proteins in vivo or in vitro.

Highlighted Text: Show | Hide
Loading full text...

Full text loading...

Comment has been disabled for this content
Submit comment
Close
Comment moderation successfully completed

Figures

Image of Figure 1
Figure 1

Citation: Csonka L, Leisinger T. 2007. Biosynthesis of Proline, EcoSal Plus 2007; doi:10.1128/ecosalplus.3.6.1.4
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of Figure 2
Figure 2

to are the genes for the enzymes catalyzing the first five reactions of arginine biosynthesis. The gene specifies a bifunctional dehydrogenase that oxidizes proline to P5C (proline dehydrogenase) and P5C into glutamate (P5C dehydrogenase). FAD, flavin adenine dinucleotide; FADH2, reduced flavin adenine dinucleotide.

Citation: Csonka L, Leisinger T. 2007. Biosynthesis of Proline, EcoSal Plus 2007; doi:10.1128/ecosalplus.3.6.1.4
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of Figure 3
Figure 3

The sequences used for this comparison correspond to the strains listed in Table 2. For each strain, the pairs of sequences highlighted with yellow, green, or pink backgrounds are inverted repeats. Asterisks indicate residues that are conserved across the species in each group.

(B) Promoter regions of the gene. The boxed sequences TTGCCT and TATGCT are possible −35 and −10 elements of the promoter in . and (see the text). (i) For . , , and . serovar Typhimurium, the boxed sequence CAT in green shows the translation start site of the neighboring gene , read in the opposite direction from . For and (ii), , , and (iii), and (iv), the boxed sequences TAA, TGA, and TAG in red are the translation stop codons for the upstream gene.

The inverted repeat sequences in Fig. 3 and 4 were identified with the program Stemmer. We acknowledge P. T. Gilham (Department of Biological Sciences, Purdue University) for help with this algorithm. (A) Promoter regions of the operon. The boxed sequences TTGGCA and TAAAAC, TACAAC, and TACAAA are proposed as the −35 and −10 components of the promoter (see the text). The boxed ATG sequence in green is the translation start site. The sequences from and are identical in the region shown.

Citation: Csonka L, Leisinger T. 2007. Biosynthesis of Proline, EcoSal Plus 2007; doi:10.1128/ecosalplus.3.6.1.4
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of Figure 4
Figure 4

The pairs of sequences highlighted with a yellow background are inverted repeats, with allowance for possible G-U pairing in the mRNA. Runs of T’s (U’s in mRNA) are highlighted in orange. Asterisks indicate nucleotides that are conserved across the species in each group.

(A) Terminator regions of the operon. The boxed TAA and TGA sequences in red are the translation termination codons of the gene. The sequences from . and are identical in the region shown. Asterisks indicate nucleotides that are conserved in . , , and . serovar Typhimurium (i) and in , , and (ii). Plus signs indicate nucleotides that are conserved between and , and exclamation marks show nucleotides that are conserved among all four species listed in panel ii. (B) terminator regions. (i) For . , , and . serovar Typhimurium, the boxed TGA sequence in red is the translation terminator for the gene and the boxed TCA sequence in red is the translation terminator for the downstream () gene, read toward . The sequences from . and are identical in this region. (ii) For , , , , and (ii) and for (iii), the boxed TGA and TGA sequences in red are the termination codons for and the boxed ATG sequence in green is the initiator for the next downstream gene. Asterisks indicate the nucleotides conserved among , , , and , plus signs indicate nucleotides conserved between and , and exclamation marks indicate nucleotides that are conserved among all five of these species. nt, nucleotides.

The inverted repeat sequences were identified with the program Stemmer.

Citation: Csonka L, Leisinger T. 2007. Biosynthesis of Proline, EcoSal Plus 2007; doi:10.1128/ecosalplus.3.6.1.4
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of Figure 5
Figure 5

The sequences of the respective three genes are 100% identical between the two organisms. The sequences highlighted with various colored backgrounds are inverted repeats that can form stem structures. Asterisks indicate nucleotides that are conserved in all three tRNAs.

Citation: Csonka L, Leisinger T. 2007. Biosynthesis of Proline, EcoSal Plus 2007; doi:10.1128/ecosalplus.3.6.1.4
Permissions and Reprints Request Permissions
Download as Powerpoint

Tables

Generic image for table
Table 1

Genes and gene products of proline metabolism in . and

Citation: Csonka L, Leisinger T. 2007. Biosynthesis of Proline, EcoSal Plus 2007; doi:10.1128/ecosalplus.3.6.1.4
Generic image for table
Table 2

Comparison of the predicted amino acid and nucleotide sequences of the proline biosynthesis genes of

Citation: Csonka L, Leisinger T. 2007. Biosynthesis of Proline, EcoSal Plus 2007; doi:10.1128/ecosalplus.3.6.1.4
Generic image for table
Table 3

Proline analogs

Citation: Csonka L, Leisinger T. 2007. Biosynthesis of Proline, EcoSal Plus 2007; doi:10.1128/ecosalplus.3.6.1.4

Supplemental Material

No supplementary material available for this content.

This is a required field
Please enter a valid email address
Please check the format of the address you have entered.
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error